Manipulating reproductive effort leads to changes in female reproductive scheduling but not oxidative stress

The trade‐off between reproductive investment and lifespan is the single most important concept in life‐history theory. A variety of sources of evidence support the existence of this trade‐off, but the physiological costs of reproduction that underlie this relationship remain poorly understood. The Free Radical Theory of Ageing suggests that oxidative stress, which occurs when there is an imbalance between the production of damaging Reactive Oxygen Species (ROS) and protective antioxidants, may be an important mediator of this trade‐off. We sought to test this theory by manipulating the reproductive investment of female mice (Mus musculus domesticus) and measuring the effects on a number of life history and oxidative stress variables. Females with a greater reproductive load showed no consistent increase in oxidative damage above females who had a smaller reproductive load. The groups differed, however, in their food consumption, reproductive scheduling and mean offspring mass. Of particular note, females with a very high reproductive load delayed blastocyst implantation of their second litter, potentially mitigating the costs of energetically costly reproductive periods. Our results highlight that females use strategies to offset particularly costly periods of reproduction and illustrate the absence of a simple relationship between oxidative stress and reproduction.     

Effects of developmental conditions on growth,stress and telomeres in black‐legged kittiwake chicks

Early‐life conditions can drive ageing patterns and life history strategies throughout the lifespan. Certain social, genetic and nutritional developmental conditions are more likely to produce high‐quality offspring: those with good likelihood of recruitment and productivity. Here, we call such conditions “favoured states” and explore their relationship with physiological variables during development in a long‐lived seabird, the black‐legged kittiwake (Rissa tridactyla). Two favoured states were experimentally generated by manipulation of food availability and brood size, while hatching order and sex were also explored as naturally generating favoured states. Thus, the favoured states we explored were high food availability, lower levels of sibling competition, hatching first and male sex. We tested the effects of favoured developmental conditions on growth, stress, telomere length (a molecular marker associated with lifespan) and nestling survival. Generation of favoured states through manipulation of both the nutritional and social environments furthered our understanding of their relative contributions to development and phenotype: increased food availability led to larger body size, reduced stress and higher antioxidant status, while lower sibling competition (social environment) led to lower telomere loss and longer telomere lengths in fledglings. Telomere length predicted nestling survival, and wing growth was also positively correlated with telomere length, supporting the idea that telomeres may indicate individual quality, mediated by favoured states.     

Sex‐specific telomere length and dynamics in relation to age and reproductive success in Cory’s shearwaters

Individuals in free‐living animal populations generally differ substantially in reproductive success, lifespan and other fitness‐related traits, but the molecular mechanisms underlying this variation are poorly understood. Telomere length and dynamics are candidate traits explaining this variation, as long telomeres predict a higher survival probability and telomere loss has been shown to reflect experienced “life stress.” However, telomere dynamics among very long‐lived species are unresolved. Additionally, it is generally not well understood how telomeres relate to reproductive success or sex. We measured telomere length and dynamics in erythrocytes to assess their relationship to age, sex and reproduction in Cory's shearwaters (Calonectris borealis), a long‐lived seabird, in the context of a long‐term study. Adult males had on average 231 bp longer telomeres than females, independent of age. In females, telomere length changed relatively little with age, whereas male telomere length declined significantly. Telomere shortening within males from one year to the next was three times higher than the interannual shortening rate based on cross‐sectional data of males. Past long‐term reproductive success was sex‐specifically reflected in age‐corrected telomere length: males with on average high fledgling production were characterized by shorter telomeres, whereas successful females had longer telomeres, and we discuss hypotheses that may explain this contrast. In conclusion, telomere length and dynamics in relation to age and reproduction are sex‐dependent in Cory's shearwaters and these findings contribute to our understanding of what characterises individual variation in fitness.     

The role of fecundity and reproductive effort in defining life‐history strategies of North American freshwater mussels

Selection is expected to optimize reproductive investment resulting in characteristic trade‐offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life‐history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life‐history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life‐history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life‐history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade‐off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade‐off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life‐history strategies. Combined with trade‐offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r‐selected species (e.g. tribe Anodontini and some Lampsilini) to K‐selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life‐history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.     

Life span and reproductive cost explain interspecific variation in the optimal onset of reproduction

Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR–fitness relationship only has been investigated intraspecifically. Here, we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species‐specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life history as well as social and ecological factors. Most individuals adopted the species‐specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with life span. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long life span and costs of early reproduction. By providing the first empirical confirmations of key predictions of life‐history theory across species, this study contributes to a better understanding of life‐history evolution.     

Behavioural,physiological and molecular changes in alloparental caregivers may be responsible for selection response for female reproductive investment in honey bees

Reproductive investment is a central life history variable that influences all aspects of life. Hormones coordinate reproduction in multicellular organisms, but the mechanisms controlling the collective reproductive investment of social insects are largely unexplored. One important aspect of honey bee (Apis mellifera) reproductive investment consists of raising female‐destined larvae into new queens by alloparental care of nurse bees in form of royal jelly provisioning. Artificial selection for commercial royal jelly production over 40 years has increased this reproductive investment by an order of magnitude. In a cross‐fostering experiment, we establish that this shift in social phenotype is caused by nurse bees. We find no evidence for changes in larval signalling. Instead, the antennae of the nurse bees of the selected stock are more responsive to brood pheromones than control bees. Correspondingly, the selected royal jelly bee nurses are more attracted to brood pheromones than unselected control nurses. Comparative proteomics of the antennae from the selected and unselected stocks indicate putative molecular mechanisms, primarily changes in chemosensation and energy metabolism. We report expression differences of several candidate genes that correlate with the differences in reproductive investment. The functional relevance of these genes is supported by demonstrating that the corresponding proteins can competitively bind one previously described and one newly discovered brood pheromone. Thus, we suggest several chemosensory genes, most prominently OBP16 and CSP4, as candidate mechanisms controlling queen rearing, a key reproductive investment, in honey bees. These findings reveal novel aspects of pheromonal communication in honey bees and explain how sensory changes affect communication and lead to a drastic shift in colony‐level resource allocation to sexual reproduction. Thus, pheromonal and hormonal communication may play similar roles for reproductive investment in superorganisms and multicellular organisms, respectively.     

Lifespan and age,but not residual reproductive value or condition,are related to behaviour in wild field crickets

Individuals frequently show long‐term consistency in behaviour over their lifetimes, referred to as “personality.” Various models, revolving around the use of resources and how they are valued by individuals, attempt to explain the maintenance of these different behavioural types within a population, and evaluating them is the key for understanding the evolution of behavioural variation. The pace‐of‐life syndrome hypothesis suggests that differences in personalities result from divergent life‐history strategies, with more active/risk‐taking individuals reproducing rapidly but dying young. However, studies of wild animals provide only limited support for key elements of this and related hypotheses, such as a negative relationship between residual reproductive value and activity. Furthermore, alternative models make divergent predictions regarding the relationship between risk‐taking behaviours and variables consistent in the short‐term, such as condition. To test these predictions, we regularly measured willingness to leave a shelter and the activity level of wild adult field crickets (Gryllus campestris) at both short and long intervals over their entire adult lives. We found some support for a pace‐of‐life syndrome influencing personality, as lifespan was negatively related to willingness to leave the shelter and activity. Crickets did not appear to protect their “assets” however, as estimates of residual reproductive value were not related to behaviour. Although there was considerable variance attributed to the short‐term consistency, neither trait was affected by phenotypic condition, failing to support either of the models we tested. Our study confirms that behaviours may covary with some life‐history traits and highlights the scales of temporal consistency that are more difficult to explain.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.     

Sex differences in the effects of juvenile and adult diet on age‐dependent reproductive effort

Sexual selection should cause sex differences in patterns of resource allocation. When current and future reproductive effort trade off, variation in resource acquisition might further cause sex differences in age‐dependent investment, or in sensitivity to changes in resource availability over time. However, the nature and prevalence of sex differences in age‐dependent investment remain unclear. We manipulated resource acquisition at juvenile and adult stages in decorated crickets, Gryllodes sigillatus, and assessed effects on sex‐specific allocation to age‐dependent reproductive effort (calling in males, fecundity in females) and longevity. We predicted that the resource and time demands of egg production would result in relatively consistent female strategies across treatments, whereas male investment should depend sharply on diet. Contrary to expectations, female age‐dependent reproductive effort diverged substantially across treatments, with resource‐limited females showing much lower and later investment in reproduction; the highest fecundity was associated with intermediate lifespans. In contrast, long‐lived males always signalled more than short‐lived males, and male age‐dependent reproductive effort did not depend on diet. We found consistently positive covariance between male reproductive effort and lifespan, whereas diet altered this covariance in females, revealing sex differences in the benefits of allocation to longevity. Our results support sex‐specific selection on allocation patterns, but also suggest a simpler alternative: males may use social feedback to make allocation decisions and preferentially store resources as energetic reserves in its absence. Increased calling effort with age therefore could be caused by gradual resource accumulation, heightened mortality risk over time, and a lack of feedback from available mates.     

Telomere length is repeatable,shortens with age and reproductive success,and predicts remaining lifespan in a long‐lived seabird

Telomeres are protective caps at the end of chromosomes, and their length is positively correlated with individual health and lifespan across taxa. Longitudinal studies have provided mixed results regarding the within‐individual repeatability of telomere length. While some studies suggest telomere length to be highly dynamic and sensitive to resource‐demanding or stressful conditions, others suggest that between‐individual differences are mostly present from birth and relatively little affected by the later environment. This dichotomy could arise from differences between species, but also from methodological issues. In our study, we used the highly reliable Terminal Restriction Fragment analysis method to measure telomeres over a 10‐year period in adults of a long‐lived seabird, the common tern (Sterna hirundo). Telomeres shortened with age within individuals. The individual repeatability of age‐dependent telomere length was high (>0.53), and independent of the measurement interval (i.e., one vs. six years). A small (R² = .01), but significant part of the between‐individual variation in telomere length was, however, explained by the number of fledglings produced in the previous year, while reproduction in years prior to the previous year had no effect. We confirmed that age‐dependent telomere length predicted an individual's remaining lifespan. Overall, our study suggests that the majority of between‐individual variation in adult telomere length is consistent across adult life, and that a smaller part of the variation can be explained by dynamic factors, such as reproduction.     

Evolution of increased competitiveness in cows trades off with reduced milk yield,fertility and more masculine morphology

In some species females compete for food, foraging territories, mating, and nesting sites. Competing females can exhibit morphological, physiological, and behavioral adaptations typical of males, which are commonly considered as secondary sexual traits. Competition and the development of traits increasing competitiveness require much energy and may exert adverse effects on fecundity and survival. From an evolutionary perspective, positive selection for increased competitiveness would then result in evolution of reduced values for traits related to fitness such as fecundity and survival. There is recent evidence for such evolutionary trade‐offs involving male competition, but no study has considered competing females so far. Using data from competitions for dominance in cows (Bos taurus), we found negative genetic correlations between traits providing success in competition, that is, fighting ability and fitness traits related to milk production and with fertility (the inverse of parity‐conception interval). Fighting ability also showed low but positive genetic correlations with “masculine” morphological traits, and negative correlations with “feminine” traits. A genetic change in traits over time has occurred due to selection on competitiveness, corresponding to an evolutionary process of “masculinization” counteracting the official selection for milk yield. Similar evolutionary trade‐off between success in competition and fitness components may be present in various species experiencing female competition.     

Hematocrit,age, and survival in a wild vertebrate population

Understanding trade‐offs in wild populations is difficult, but important if we are to understand the evolution of life histories and the impact of ecological variables upon them. Markers that reflect physiological state and predict future survival would be of considerable benefit to unraveling such trade‐offs and could provide insight into individual variation in senescence. However, currently used markers often yield inconsistent results. One underutilized measure is hematocrit, the proportion of blood comprising erythrocytes, which relates to the blood's oxygen‐carrying capacity and viscosity, and to individual endurance. Hematocrit has been shown to decline with age in cross‐sectional studies (which may be confounded by selective appearance/disappearance). However, few studies have tested whether hematocrit declines within individuals or whether low hematocrit impacts survival in wild taxa. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we demonstrated that hematocrit increases with age in young individuals (<1.5 years) but decreases with age in older individuals (1.5–13 years). In breeders, hematocrit was higher in males than females and varied relative to breeding stage. High hematocrit was associated with lower survival in young individuals, but not older individuals. Thus, while we did not find support for hematocrit as a marker of senescence, high hematocrit is indicative of poor condition in younger individuals. Possible explanations are that these individuals were experiencing dehydration and/or high endurance demands prior to capture, which warrants further investigation. Our study demonstrates that hematocrit can be an informative metric for life‐history studies investigating trade‐offs between survival, longevity, and reproduction.     

Density‐dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size

Most life forms exhibit a correlated evolution of adult size (AS) and size at independence (SI), giving rise to AS–SI scaling relationships. Theory suggests that scaling arises because relatively large adults have relatively high reproductive output, resulting in strong density‐dependent competition in early life, where large size at independence provides a competitive advantage to juveniles. The primary goal of our study is to test this density hypothesis, using large datasets that span the vertebrate tree of life (fishes, amphibians, reptiles, birds, and mammals). Our secondary goal is to motivate new hypotheses for AS–SI scaling by exploring how subtle variation in life‐histories among closely related species is associated with variation in scaling. Our phylogenetically informed comparisons do not support the density hypothesis. Instead, exploration of AS–SI scaling among life‐history variants suggests that steeper AS–SI scaling slopes are associated with evolutionary increases in size at independence. We suggest that a positive association between size at independence and juvenile growth rate may represent an important mechanism underlying AS–SI scaling, a mechanism that has been underappreciated by theorists. If faster juvenile growth is a consequence of evolutionary increases in size at independence, this may help offset the cost of delayed maturation, leading to steeper AS–SI scaling slopes.     

Reconciling nutritional geometry with classical dietary restriction: Effects of nutrient intake,not calories,on survival and reproduction

Dietary restriction (DR) is one of the main experimental paradigms to investigate the mechanisms that determine lifespan and aging. Yet, the exact nutritional parameters responsible for DR remain unclear. Recently, the advent of the geometric framework of nutrition (GF) has refocussed interest from calories to dietary macronutrients. However, GF experiments focus on invertebrates, with the importance of macronutrients in vertebrates still widely debated. This has led to the suggestion of a fundamental difference in the mode of action of DR between vertebrates and invertebrates, questioning the suggestion of an evolutionarily conserved mechanism. The use of dietary dilution rather than restriction in GF studies makes comparison with traditional DR studies difficult. Here, using a novel nonmodel vertebrate system (the stickleback fish, Gasterosteus aculeatus), we test the effect of macronutrient versus calorie intake on key fitness‐related traits, both using the GF and avoiding dietary dilution. We find that the intake of macronutrients rather than calories determines both mortality risk and reproduction. Male mortality risk was lowest on intermediate lipid intakes, and female risk was generally reduced by low protein intakes. The effect of macronutrient intake on reproduction was similar between the sexes, with high protein intakes maximizing reproduction. Our results provide, to our knowledge, the first evidence that macronutrient, not caloric, intake predicts changes in mortality and reproduction in the absence of dietary dilution. This supports the suggestion of evolutionary conservation in the effect of diet on lifespan, but via variation in macronutrient intake rather than calories.     

Parasite‐associated mortality in a long‐lived mammal: Variation with host age,sex, and reproduction

Parasites can cause severe host morbidity and threaten survival. As parasites are generally aggregated within certain host demographics, they are likely to affect a small proportion of the entire population, with specific hosts being at particular risk. However, little is known as to whether increased host mortality from parasitic causes is experienced by specific host demographics. Outside of theoretical studies, there is a paucity of literature concerning dynamics of parasite‐associated host mortality. Empirical evidence mainly focuses on short‐lived hosts or model systems, with data lacking from long‐lived wild or semi‐wild vertebrate populations. We investigated parasite‐associated mortality utilizing a multigenerational database of mortality, health, and reproductive data for over 4,000 semi‐captive timber elephants (Elephas maximus), with known causes of death for mortality events. We determined variation in mortality according to a number of host traits that are commonly associated with variation in parasitism within mammals: age, sex, and reproductive investment in females. We found that potentially parasite‐associated mortality varied significantly across elephant ages, with individuals at extremes of lifespan (young and old) at highest risk. Mortality probability was significantly higher for males across all ages. Female reproducers experienced a lower probability of potentially parasite‐associated mortality than females who did not reproduce at any investigated time frame. Our results demonstrate increased potentially parasite‐associated mortality within particular demographic groups. These groups (males, juveniles, elderly adults) have been identified in other studies as susceptible to parasitism, stressing the need for further work investigating links between infection and mortality. Furthermore, we show variation between reproductive and non‐reproductive females, with mothers being less at risk of potentially parasite mortality than nonreproducers.     

Timing matters: species‐specific interactions between spawning time,substrate quality,and recruitment success in three salmonid species

Substratum quality and oxygen supply to the interstitial zone are crucial for the reproductive success of salmonid fishes. At present, degradation of spawning grounds due to fine sediment deposition and colmation are recognized as main factors for reproductive failure. In addition, changes in water temperatures due to climate change, damming, and cooling water inlets are predicted to reduce hatching success. We tested the hypothesis that the biological effects of habitat degradation depend strongly on the species‐specific spawning seasons and life‐history strategies (e.g., fall‐ vs. spring‐spawners, migratory vs. resident species) and assessed temperature as an important species‐specific factor for hatching success within river substratum. We studied the species‐specific differences in their responses to such disturbances using egg‐to‐fry survival of Danube Salmon (Hucho hucho), resident brown trout (Salmo trutta fario), and migratory brown trout (Salmo trutta lacustris) as biological endpoint. The egg incubation and hatching success of the salmonids and their dependence on temperature and stream substratum quality were compared. Hatching rates of Danube salmon were lower than of brown trout, probably due to higher oxygen demands and increased interstitial respiration in spring. Increases in maximum water temperature reduced hatching rates of resident and migratory brown trout (both fall‐spawners) but were positively correlated with hatching rates of Danube salmon (a spring‐spawner). Significantly longer incubation periods of resident and migratory brown trout coincided with relatively low stream substratum quality at the end of the egg incubation. Danube salmon seem to avoid low oxygen concentrations in the hyporheic zone by faster egg development favored by higher water temperatures. Consequently, the prediction of effects of temperature changes and altered stream substratum properties on gravel‐spawning fishes and biological communities should consider the observed species‐specific variances in life‐history strategies to increase conservation success.